Mutation of luxS affects motility and infectivity of Helicobacter pylori in gastric mucosa of a Mongolian gerbil model

Journal of Medical Microbiology

Volumn 55, Issue 11, 2006, Pages 1477-1485

  Osaki, Takako ^a   Hanawa, Tomoko ^a   Manzoku, Taki ^a   Fukuda, Minoru ^a   Kawakami, Hayato ^a   Suzuki, Hidekazu ^b   Yamaguchi, Hiroyuki ^c   Yan, Xu ^d   Taguchi, Haruhiko ^a   Kurata, Satoshi ^a   Kamiya, Shigeru ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d Kunming Medical University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIUM MUTANT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GASTRITIS; GENE MUTATION; GERBIL; HELICOBACTER PYLORI; HISTOPATHOLOGY; LUXS GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; STOMACH MUCOSA;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CARBON-SULFUR LYASES; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; FLAGELLA; GASTRIC MUCOSA; GERBILLINAE; GLUCOSE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOMOSERINE; HUMANS; HYDROGEN-ION CONCENTRATION; LACTONES; MALE; MICROSCOPY, ELECTRON, SCANNING; MUTAGENESIS, INSERTIONAL; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STOMACH DISEASES;

EID: 33750838005     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.46660-0     Document Type: Article

References (45)

1. Balestrino, D., Haagensen, J. A., Rich, C. & Forestier, C. (2005). Characterization of type 2 quorum sensing in Klebsiella pneumoniae and relationship with biofilm formation. J Bacteriol 187, 2870-2880.
2. Blaser, M. J. (1992). Helicobacter pylori: its role in disease. Clin Infect Dis 15, 386-391.
3. Blehert, D. S., Palmer, R. J., Jr, Xavier, J. B., Almeida, J. S. & Kolenbrander, P. E. (2003). Autoinducer 2 production by Streptococcus gordonii DL1 and the biofilm phenotype of a luxS mutant are influenced by nutritional conditions. J Bacteriol 185, 4851-4860.
4. Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B. L. & Hughson, F. M. (2002). Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415, 545-549.
5. Drazek, E. S., Dubois, A. & Holmes, R. K. (1994). Characterization and presumptive identification of Helicobacter pylori isolates from rhesus monkeys. J Clin Microbiol 32, 1799-1804.
6. Eaton, K. A., Suerbaum, S., Josenhans, C. & Krakowka, S. (1996). Colonization of gnotobiotic piglets by Helicobacter pylori deficient in two flagellin genes. Infect Immun 64, 2445-2448.
7. Eaton, K. A., Cover, T. L., Tummuru, M. K. R., Blaser, M. J. & Krakowka, S. (1997). Role of vacuolating cytotoxin in gastritis due to Helicobacter pylori in gnotobiotic piglets. Infect Immun 65, 3462-3464.
8. Evans, D. G., Karjalainen, T. K., Evans, D. J., Graham, D. Y. & Lee, C. H. (1993). Cloning, nucleotide sequence, and expression of a gene encoding an adhesin subunit protein of Helicobacter pylori. J Bacteriol 175, 674-683.
9. Falk, P., Roth, K. A., Boren, T., Westblom, T. U., Gordon, J. I. & Normark, S. (1993). An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineage-specific tropism in the human gastric epithelium. Proc Natl Acad Sci U S A 90, 2035-2039.
10. Fong, K. P., Chung, W. O., Lamont, R. J. & Demuth, D. R. (2001). Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect Immun 69, 7625-7634.
11. Forsyth, M. H. & Cover, T. L. (2000). Intercellular communication in Helicobacter pylori: luxS is essential for the production of an extracellular signaling molecule. Infect Immun 68, 3193-3199.
12. Fujioka, T., Kodama, R., Honda, S., Guei-Hua, G., Nishizono, A. & Nasu, M. (1997). Long-term sequelae of experimental gastritis with Helicobacter pylori: a 5-year follow-up study. J Clin Gastroenterol 25 (Suppl. 1), S8-S12.
13. Fuqua, W. C., Winans, S. C. & Greenberg, E. P. (1994). Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176, 269-275.
14. Graham, D. Y. (1989). Campylobacter pylori and peptic ulcer disease. Gastroenterology 96, 615-625.
15. Hardie, K. R., Cooksley, C., Green, A. D. & Winzer, K. (2003). Auto-inducer 2 activity in Escherichia coli culture supernatants can be actively reduced despite maintenance of an active synthase. Microbiology 149, 715-728.
16. Hirayama, F., Takagi, S., Yokoyama, Y., Iwao, E. & Ikeda, Y. (1996). Establishment of gastric Helicobacter pylori infection in Mongolian gerbils. J Gastroenterol 31, 24-28.
17. Iwao, E., Hirayama, F., Takagi, S., Yokoyama, Y. & Ikeda, Y. (1999). Virulence factors of Helicobacter pylori affecting its gastric colonization in Mongolian gerbils. J Gastroenterol 34 (Suppl. 11), 47-54.
18. Jeon, B., Itoh, K., Misawa, N. & Ryu, S. (2003). Effects of quorum sensing on flaA transcription and autoagglutination in Campylobacter jejuni. Microbiol Immunol 47, 833-839.
19. Joyce, E. A., Bassler, B. L. & Wright, A. (2000). Evidence for a signaling system in Helicobacter pylori: detection of a luxS-encoded autoinducer. J Bacteriol 182, 3638-3643.
20. Kim, S. Y., Lee, S. E., Kim, Y. R., Kim, C. M., Ryu, P. Y., Choy, H. E., Chung, S. S. & Rhee, J. H. (2003). Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol Microbiol 48, 1647-1664.
21. Lee, A., O'Rourke, J., Ungria, M. C. D., Robertson, B., Daskalopoulos, G. & Dixon, M. F. (1997). A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112, 1386-1397.
22. Loh, J. T., Forsyth, M. H. & Cover, T. L. (2004). Growth phase regulation of flaA expression in Helicobacter pylori is luxS dependent. Infect Immun 72, 5506-5510.
23. Lyon, W. R., Madden, J. C., Levin, J. C., Stein, J. L. & Caparon, M. G. (2001). Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42, 145-157.
24. Marshall, B. J. & Warren, J. R. (1984). Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet I, 1311-1315.
25. Matsumoto, S., Washizuka, Y., Matsumoto, Y., Tawara, S., Ikeda, F., Yokota, Y. & Karita, M. (1997). Induction of ulceration and severe gastritis in Mongolian gerbil by Helicobacter pylori infection. J Med Microbiol 46, 391-397.
26. Nakagawa, S., Osaki, T., Fujioka, Y., Yamaguchi, H. & Kamiya, S. (2005). Long-term infection of Mongolian gerbils with Helicobacter pylori: microbiological, histopathological, and serological analyses. Clin Diagn Lab Immunol 12, 347-353.
27. Ohtani, K., Hayashi, H. & Shimizu, T. (2002). The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Mol Microbiol 44, 171-179.
28. Osaki, T., Taguchi, H., Yamaguchi, H., Kumada, J., Ogata, S. & Kamiya, S. (1997). Studies on the relationship between adhesive activity and haemagglutination by Helicobacter pylori. J Med Microbiol 46, 117-121.
29. Osaki, T., Taguchi, H., Yamaguchi, H. & Kamiya, S. (1998). Detection of Helicobacter pylori in fecal samples of gnotobiotic mice infected with H. pylori by an immunomagnetic-bead separation technique. J Clin Microbiol 36, 321-323.
30. O'Toole, P. W., Janzon, L., Doig, P., Huang, J. Z., Kostrzynska, M. & Trust, T. J. (1995). The putative neuraminyllactose-binding hemagglutinin HpaA of Helicobacter pylori CCUG 17874 is a lipoprotein. J Bacteriol 177, 6049-6057.
31. Personnel, J., Friedman, G. D., Vandersteen, D. P., Chang, Y., Vogelman, J. H, & Orentreich, N. (1991). Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325, 1127-1131.
32. Salama, N. R., Otto, G., Tompkins, L. & Falkow, S. (2001). Vacuolating cytotoxin of Helicobacter pylori plays a role during colonization in a mouse model of infection. Infect Immun 69, 730-736.
33. Schauder, S., Shokat, K., Surette, M. G. & Bassler, B. L. (2001). The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41, 463-176.
34. Schneider, R., Lockatell, C. V., Johnson, D. & Belas, R. (2002). Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology 148, 773-782.
35. Sircili, M. P., Walters, M., Trabulsi, L. R. & Sperandio, V. (2004). Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect Immun 72, 2329-2337.
36. Sperandio, V., Mellies, J. L., Nguyen, W., Shin, S. & Kaper, J. B. (1999). Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 96, 15196-15201.
37. Stroeher, U. H., Paton, A. W., Ogunniyi, A. D. & Paton, J. C. (2003). Mutation of luxS of Streptococcus pneumoniae affects virulence in a mouse model. Infect Immun 71, 3206-3212.
38. Surette, M. G. & Bassler, B. L. (1999). Regulation of autoinducer production in Salmonella typhimurium. Mol Microbiol 31, 585-595.
39. Thompson, L. J., Merrell, D. S., Neilan, B. A., Mitchell, H., Lee, A. & Falkow, S. (2003). Gene expression profiling of Helicobacter pylori reveals a growth-phase-dependent switch in virulence gene expression. Infect Immun 71, 2643-2655.
40. Tsuda, M., Karita, M., Morshed, M. G., Okita, K. & Nakazawa, T. (1994). A urease-negative mutant of Helicobacter pylori constructed by allelic exchange mutagenesis lacks the ability to colonize the nude mouse stomach. Infect Immun 62, 3586-3589.
41. Wen, Z. T. & Burne, R. A. (2004). LuxS-mediated signaling in Streptococcus mutans is involved in regulation of acid and oxidative stress tolerance and biofilm formation. J Bacteriol 186, 2682-2691.
42. Wotherspoon, A. C., Doglioni, C., Diss, T. C., Pan, L, Moschini, A., De Boni, M. & Isaacson, P. G. (1993). Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet 342, 575-577.
43. Yamaguchi, H., Osaki, T., Kai, M., Taguchi, H. & Kamiya, S. (2000). Immune response against a cross-reactive epitope on the heat shock protein 60 homologue of Helicobacter pylori. Infect Immun 68, 3448-3454.
44. Yamaoka, Y., Kita, M., Kodama, T., Imamura, S., Ohno, T., Sawai, N., Ishimaru, A., Imanishi, J. & Graham, D. Y. (2002). Helicobacter pylori infection in mice: role of outer membrane proteins in colonization and inflammation. Gastroenterology 123, 1992-2004.
45. Yokota, K., Kurebayashi, Y., Takayama, Y. & 7 other authors (1991). Colonization of Helicobacter pylori in the gastric mucosa of Mongolian gerbils. Microbiol Immunol 35, 475-480.